Inoviridae prophage and bacterial host dynamics during diversification, succession, and Atlantic invasion of Pacific-native Vibrio parahaemolyticus

Abstract

The epidemiology of Vibrio parahaemolyticus , the leading cause of seafood-borne bacterial gastroenteritis of humans worldwide, dramatically changed in the United States following the establishment of a Pacific-native lineage called sequence type (ST) 36 in the Atlantic. In this study, we used phylogeography based on traceback to environmental source locations and comparative genomics to identify features that promoted evolution, dispersal, and competitive dominance of ST36. The major genomic differentiation and competitive success of ST36 were associated with a striking succession of filamentous prophage in the family Inoviridae (inoviruses), including loss of an inovirus prophage that had been maintained for decades in the endemic north Pacific population. Subsequently, at least five distinct progenitors arising from this diversification translocated from the Pacific into the Atlantic and established four geographically defined clonal subpopulations with remarkably low migration or mixing. Founders of two prevailing Atlantic subpopulations each acquired new stable and diagnostic inoviruses while other subpopulations that apparently declined did not. Broader surveys indicate inoviruses are common and active among the global population of V. parahaemolyticus , and though inovirus replacements, such as in ST36, appear to be infrequent, they are notable in pathogenic lineages that dispersed. IMPORTANCE An understanding of the processes that contribute to the emergence of pathogens from environmental reservoirs is critical as changing climate precipitates pathogen evolution and population expansion. Phylogeographic analysis of Vibrio parahaemolyticus hosts combined with the analysis of their Inoviridae phage resolved ambiguities of diversification dynamics which preceded successful Atlantic invasion by the epidemiologically predominant ST36 lineage. It has been established experimentally that filamentous phage can limit host recombination, but here, we show that phage loss is linked to rapid bacterial host diversification during epidemic spread in natural ecosystems alluding to a potential role for ubiquitous inoviruses in the adaptability of pathogens. This work paves the way for functional analyses to define the contribution of inoviruses in the evolutionary dynamics of environmentally transmitted pathogens.

Complete genome sequence of Vibrio parahaemolyticus ST36 strain MAVP-26, a clinical isolate from an oyster-borne human gastric infection

“…The introduction of Pacific native V. parahaemolyticus into the North Atlantic has raised concerns about how the non-native V. parahaemolyticus may evolve under local selection or even spur the evolution of new variants by recombination with endemic lineages ( 1 – 6 ). This is especially concerning considering that Vibrio pathogenicity islands (VPaI), which confer disease in humans ( 7 ), are mobile by nature.…”

“…Therefore, we sequenced reference strain MAVP-26, a 2013 clinical isolate ( 8 , 9 ). The vector of the gastric illness was a commercial oyster definitively traced to a harvest area in Cape Cod Bay (42.0201° N; 70.6514° W), where the lineage is now established ( 2 ).…”

“…The genome contains two circular chromosomes, chromosome I (3,360,050 bp) and chromosome II (1.849,390 bp), encoding 5,047 genes with 45.5% GC content. Notable mobile elements including the pathogenicity island (VPaI-γ) and inovirus ( 1 , 2 ) and other diagnostic features ( 9 ) are indicated ( Fig. 1 ).…”

“…This Whole Genome Shotgun project has been deposited in GenBank under the accession number CP023248 (chromosome I) and CP023247 (Chromosome II). The PacBio raw reads are available under the accession number SRR28518279, and the Illumina short reads are available under the accession number SRS893228 ( 2 ). This is the second version of the complete hybrid assembly genome of V. parahaemolyticus MAVP-26, and in addition to the previous hybrid assembly, a prior assembly (30 contigs, N50 = 809,100) from the Illumina reads was previously released under the RefSeq accession number GCF_001023055.1 and GenBank WGS is LBHD00000000.1 ( 2 ).…”